ABSTRACT Evolutionary genomic approaches provide powerful tools to understand variation in and evolution of physiological processes. Untargeted genomic or transcriptomic screens can identify functionally annotated candidate genes linked to specific physiological processes, in turn suggesting evolutionary roles for these processes. Such studies often aim to inform modeling of the potential of natural populations to adapt to climate change, but these models are most accurate when evolutionary responses are repeatable, and thus predictable. Here, we synthesize the evolutionary genetic and comparative transcriptomic literature on terrestrial and marine invertebrates to assess whether evolutionary responses to temperature are repeatable within populations, across populations and across species. There is compelling evidence for repeatability, sometimes even across species. However, responses to laboratory selection and geographic variation across thermal gradients appear to be highly idiosyncratic. We also survey whether genetic/transcriptomic studies repeatedly identify candidate genes in three functional groups previously associated with the response to thermal stress: heat shock protein (Hsp) genes, proteolysis genes and immunity genes. Multiple studies across terrestrial and marine species identify candidates included in these gene sets. Yet, each of the gene sets are identified in only a minority of studies. Together, these patterns suggest that there is limited predictability of evolutionary responses to natural selection, including across studies within species. We discuss specific patterns for the candidate gene sets, implications for predictive modeling, and other potential applications of evolutionary genetics in elucidating physiology and gene function. Finally, we discuss limitations of inferences from available evolutionary genetic studies and directions for future research.
more »
« less
Evolution repeats itself in replicate long-term studies in the wild
The extent to which evolution is repeatable remains debated. Here, we study changes over time in the frequency of cryptic color-pattern morphs in 10 replicate long-term field studies of a stick insect, each spanning at least a decade (across 30 years of total data). We find predictable “up-and-down” fluctuations in stripe frequency in all populations, representing repeatable evolutionary dynamics based on standing genetic variation. A field experiment demonstrates that these fluctuations involve negative frequency-dependent natural selection (NFDS). These fluctuations rely on demographic and selective variability that pushes populations away from equilibrium, such that they can reliably move back toward it via NFDS. Last, we show that the origin of new cryptic forms is associated with multiple structural genomic variants such that which mutations arise affects evolution at larger temporal scales. Thus, evolution from existing variation is predictable and repeatable, but mutation adds complexity even for traits evolving deterministically under natural selection.
more »
« less
- Award ID(s):
- 1844941
- PAR ID:
- 10584195
- Publisher / Repository:
- AAAS
- Date Published:
- Journal Name:
- Science Advances
- Volume:
- 10
- Issue:
- 21
- ISSN:
- 2375-2548
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract How repeatable is evolution at genomic and phenotypic scales? We studied the repeatability of evolution during 8 generations of colonization using replicated microcosm experiments with the red flour beetle, Tribolium castaneum. Based on the patterns of shared allele frequency changes that occurred in populations from the same generation or experimental location, we found adaptive evolution to be more repeatable in the introduction and establishment phases of colonization than in the spread phase, when populations expand their range. Lastly, by studying changes in allele frequencies at conserved loci, we found evidence for the theoretical prediction that range expansion reduces the efficiency of selection to purge deleterious alleles. Overall, our results increase our understanding of adaptive evolution during colonization, demonstrating that evolution can be highly repeatable while also showing that stochasticity still plays an important role.more » « less
-
The influence of genetic drift on population dynamics during Pleistocene glacial cycles is well understood, but the role of selection in shaping patterns of genomic variation during these events is less explored. We resequenced whole genomes to investigate how demography and natural selection interact to generate the genomic landscapes of Downy and Hairy Woodpecker, species codistributed in previously glaciated North America. First, we explored the spatial and temporal patterns of genomic diversity produced by neutral evolution. Next, we tested (i) whether levels of nucleotide diversity along the genome are correlated with intrinsic genomic properties, such as recombination rate and gene density, and (ii) whether different demographic trajectories impacted the efficacy of selection. Our results revealed cycles of bottleneck and expansion, and genetic structure associated with glacial refugia. Nucleotide diversity varied widely along the genome, but this variation was highly correlated between the species, suggesting the presence of conserved genomic features. In both taxa, nucleotide diversity was positively correlated with recombination rate and negatively correlated with gene density, suggesting that linked selection played a role in reducing diversity. Despite strong fluctuations in effective population size, the maintenance of relatively large populations during glaciations may have facilitated selection. Under these conditions, we found evidence that the individual demographic trajectory of populations modulated linked selection, with purifying selection being more efficient in removing deleterious alleles in large populations. These results highlight that while genome-wide variation reflects the expected signature of demographic change during climatic perturbations, the interaction of multiple processes produces a predictable and highly heterogeneous genomic landscape.more » « less
-
Abstract Populations declining due to climate change may need to evolve to persist. While evolutionary rescue has been demonstrated in theory and the lab, its relevance to natural populations facing climate change remains unknown. Here we link rapid evolution and population dynamics in scarlet monkeyflower,Mimulus cardinalis, during an exceptional drought. We leverage whole-genome sequencing across 55 populations to identify climate-associated loci. Simultaneously we track demography and allele frequency change throughout the drought. We establish range-wide population decline during the drought, geographically variable rapid evolution, and variable population recovery that is predictable by both standing genetic variation and rapid evolution at climate-associated loci. These findings demonstrate evolutionary rescue in the wild, showing that genomic variability at adaptive, but not neutral loci, predicts population recovery.more » « less
-
Abstract Circadian clocks confer adaptation to predictable 24‐h fluctuations in the exogenous environment, but it has yet to be determined what ecological factors maintain natural genetic variation in endogenous circadian period outside of the hypothesized optimum of 24 h. We estimated quantitative genetic variation in circadian period in leaf movement in 30 natural populations of theArabidopsisrelativeBoechera strictasampled within only 1° of latitude but across an elevation gradient spanning 2460–3300 m in the Rocky Mountains. Measuring ~3800 plants from 473 maternal families (7–20 per population), we found that genetic variation was of similar magnitude among versus within populations, with population means varying between 21.9 and 24.9 h and maternal family means within populations varying by up to ~6 h. After statistically accounting for spatial autocorrelation at a habitat extreme, we found that elevation explained a significant proportion of genetic variation in the circadian period, such that higher‐elevation populations had shorter mean period lengths and reduced intrapopulation ranges. Environmental data indicate that these spatial trends could be related to steep regional climatic gradients in temperature, precipitation, and their intra‐annual variability. Our findings suggest that spatially fine‐grained environmental heterogeneity contributes to naturally occurring genetic variation in circadian traits in wild populations.more » « less
An official website of the United States government

